In Situ Hydrogen and Nitrous Oxide as Indicators of Concomitant Fermentation and Denitrification in the Alimentary Canal of the Earthworm Lumbricus terrestris

The earthworm gut is a unique microzone in aerated soils that has been proposed to selectively stimulate ingested soil microorganisms by its in situ conditions, which include anoxia, high water content, a near-neutral pH, and high concentrations of organic compounds. The central objective of this st...

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Bibliographic Details
Published in:Applied and Environmental Microbiology 2009-04, Vol.75 (7), p.1852-1859
Main Authors: Wüst, Pia K, Horn, Marcus A, Drake, Harold L
Format: Article
Language:English
Subjects:
Acetic acid
Animals
Biological and medical sciences
Biotechnology
Carbon - analysis
Carboxylic Acids - analysis
Chemical compounds
Digestive System - chemistry
Digestive System - microbiology
Fermentation
Ferric Compounds - analysis
Fundamental and applied biological sciences. Psychology
Hydrogen
Hydrogen - analysis
Invertebrate Microbiology
Lumbricus terrestris
Methods. Procedures. Technologies
Microbial engineering. Fermentation and microbial culture technology
Microbiology
Nitrates - metabolism
Nitric oxide
Nitrites - analysis
Nitrogen - analysis
Nitrous Oxide - analysis
Oligochaeta - chemistry
Oligochaeta - microbiology
Quaternary Ammonium Compounds - analysis
Worms
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Summary:The earthworm gut is a unique microzone in aerated soils that has been proposed to selectively stimulate ingested soil microorganisms by its in situ conditions, which include anoxia, high water content, a near-neutral pH, and high concentrations of organic compounds. The central objective of this study was to resolve potential links between in situ conditions and anaerobic microbial activities during the gut passage of Lumbricus terrestris. Both H₂ and N₂O were emitted by living earthworms, and in situ microsensor analyses revealed both H₂ and N₂O in the O₂-free gut center. The highest H₂ concentrations occurred in foregut and midgut regions, whereas the highest N₂O concentrations occurred in crop/gizzard and hindgut regions. Thus, H₂-producing fermentations were more localized in the foregut and midgut, whereas denitrification was more localized in the crop/gizzard and hindgut. Moisture content, total carbon, and total nitrogen were highest in the foregut and decreased from the anterior to posterior end of the gut. Nitrite, ammonium, and iron(II) concentrations were highest in the crop/gizzard and decreased from the anterior to posterior end of the alimentary canal. Concentrations of soluble organic compounds were indicative of distinct fermentation processes along the alimentary canal, with maximal concentrations of organic acids (e.g., acetate and butyrate) occurring in the midgut. These findings suggest that earthworms (i) contribute to the terrestrial cycling of carbon and nitrogen via anaerobic microbial activities in the alimentary canal and (ii) constitute a mobile source of reductant (i.e., emitted H₂) for microbiota in aerated soils.
ISSN:0099-2240
1098-5336
1098-6596
DOI:10.1128/AEM.02745-08